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Review Fastest Predators in the Plant Kingdom: Functional Morphology and Biomechanics of Suction Traps Found in the Largest Genus of Carnivorous Plants

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Review Fastest Predators in the Plant Kingdom: Functional Morphology and Biomechanics of Suction Traps Found in the Largest Genus of Carnivorous Plants Review Fastest predators in the plant kingdom: functional morphology and biomechanics of suction traps found in the largest genus of carnivorous plants Simon Poppinga1,2*, Carmen Weisskopf1,3, Anna Sophia Westermeier1, Tom Masselter1 and Thomas Speck1,2 1 Plant Biomechanics Group, University of Freiburg, Botanic Garden, Scha¨nzlestrasse 1, 79104 Freiburg im Breisgau, Germany 2 Freiburg Materials Research Center (FMF), University of Freiburg, Stefan-Meier-Straße 21, 79104 Freiburg im Breisgau, Germany 3 Present address: Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Wissenschaftspark Potsdam-Golm, Am Mu¨hlenberg 1, 14476 Potsdam, Germany Received: 15 September 2015; Accepted: 7 November 2015; Published: 24 November 2015 Associate Editor: James F. Cahill Citation: Poppinga S, Weisskopf C, Westermeier AS, Masselter T, Speck T. 2016. Fastest predators in the plant kingdom: functional morphology and biomechanics of suction traps found in the largest genus of carnivorous plants. AoB PLANTS 8: plv140; doi:10.1093/ aobpla/plv140 Abstract. Understanding the physics of plant movements, which describe the interplay between plant architecture, movement speed and actuation principles, is essential for the comprehension of important processes like plant morphogenesis. Recent investigations especially on rapid plant movements at the interface of biology, physics and engineering sciences highlight how such fast motions can be achieved without the presence of muscles, nerves and technical hinge analogies. The suction traps (bladders) of carnivorous bladderworts (Utricularia spp., Lentibular- iaceae, Lamiales) are considered as some of the most elaborate moving structures in the plant kingdom. A complex interplay of morphological and physiological adaptations allows the traps to pump water out of their body and to store elastic energy in the deformed bladder walls. Mechanical stimulation by prey entails opening of the otherwise water- tight trapdoor, followed by trap wall relaxation, sucking in of water and prey, and consecutive trapdoor closure. Suction can also occur spontaneously in non-stimulated traps. We review the current state of knowledge about the suction trap mechanism with a focus on architectonically homogeneous traps of aquatic bladderwort species from section Utricularia (the so-called ‘Utricularia vulgaris trap type’). The functional morphology and biomechanics of the traps are described in detail. We discuss open questions and propose promising aspects for future studies on these sophis- ticated ultra-fast trapping devices. Keywords: Biomechanics; bladderwort; carnivorous plant; functional morphology; prey; suction trap; Utricularia. Introduction and can be regarded as an adaptation to a life in nutrient- Carnivorous plants attract, catch, retain and kill prey ani- poor habitats (Juniper et al. 1989; Albert et al.1992; mals and absorb the nutrients resulting from digestion Barthlott et al. 2007). Carnivorous plants are termed (Darwin 1875; Lloyd 1942). This ‘carnivorous syndrome’ ‘active’ when their traps perform motion, as, for example, has evolved several times independently in angiosperms the slow movements of Drosera (sundew) leaf blades to * Corresponding author’s e-mail address: [email protected] Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properlycited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Poppinga et al. — Functional morphology and biomechanics of Utricularia suction traps retain prey. Apart from the classical textbook division into capture and digest small prey animals with active suction taxes, tropisms, nastic and autonomous motions, such traps (Darwin 1875; Treat 1875; Lloyd 1942; reviewed by plant movements can also be described according to Guisande et al.2007). The family name can be deduced their actuation principle. Hydraulic motions function due from the Latin word for ‘lentil’ (lens), referring to the to a displacement of water between cells and tissues, lentiform traps of Utricularia, whereas the bladderwort’s which can be active (turgor changes in living cells) or pas- genus name can be ascribed to the term ‘utriculus’, sive (swelling/shrinking processes of dead cells, cohesion- which refers to the shape of a wineskin. force driven motion). The speed of hydraulic movement Bladderworts constitute the largest genus of carnivor- primarily depends on the dimension (thickness) of the ousplantsandcomprise240 species (Taylor 1989; respective plant organ which the water has to flow through Fleischmann 2012b, 2015). Molecular phylogenetic and, hence, is ultimately limited by the speed of this pro- reconstructions showed that Pinguicula holds a basal cess of water diffusion (Skotheim and Mahadevan 2005). position in the Lentibulariaceae and that Genlisea and Some active carnivorous plants have evolved traps that Utricularia are more derived sister genera (Mu¨ller et al. can move faster as theoretically possible due to pure 2000, 2004, 2006; Mu¨ller and Borsch 2005; Fleischmann hydraulics (reviewed by Forterre 2013; Poppinga et al. 2012a). The aquatic U. gibba possesses one of the smal- 2013a). A well-known example for this phenomenon is lest angiosperm genomes so far known (only rivalled the snap-trap of the Venus flytrap (Dionaea muscipula, by some species of Genlisea)(Greilhuber et al. 2006; Droseraceae), which performs a combination of stimulus- Fleischmann et al. 2014; Veleba et al. 2014), which is triggered, active hydraulic motion followed by a passive furthermore characterized by only a tiny portion of non- release of elastic energy stored in the trap lobes (snap- coding DNA (Ibarra-Laclette et al.2013). Taylor (1989) buckling) (Forterre et al. 2005). Such elastic components classified 35 sections within Utricularia according to mor- greatly boost the overall speed of the motion, which phological traits, including trap shape, position of trap otherwise would be too slow for the carnivorous plant entrance and door, and position and shape of trap appen- to overcome prey. The understanding of such mechanical dages. The molecular systematic analyses by Jobson et al. ‘tricks’ not only leads to a deepened understanding of the (2003), Mu¨ller et al. (2004) and Mu¨ller and Borsch (2005) ecology and evolution of a plant and its trapping mechan- generally corroborate this classification, and the three ism (Gibson and Waller 2009; Poppinga et al. 2013b), but subgenera Polypompholyx, Utricularia and Bivalvaria can also give great inspiration for implementation into have been proposed (Mu¨ ller et al. 2006). The sections bio-inspired technical materials (reviewed by Guo et al. Utricularia and Vesiculina (U.subgen.Utricularia)com- 2015). prise nearly all aquatic bladderworts, and the 35 species The recent proof of carnivory in Philcoxia with below- in section Utricularia share a common trap architecture ground sticky traps (Pereira et al. 2012), the discovery of (the ‘Utricularia vulgaris trap type’) (Lloyd 1935, 1942; ancient sticky trap fragments in Eocene Baltic amber Taylor 1989) that will be described in detail with all its (Sadowski et al. 2015) and comprehensive analyses of structural and functional variations in this article. Biophys- passive-dynamic prey capture mechanisms (Bauer et al. ical investigations on Utricularia have been conducted for 2015) demonstrate that carnivorous plants are always the most part on this trap type, as the respective aquatic good for ‘a surprise’. In this review, we summarize the species possess relative large traps and are comparably current state of knowledge about the fastest active trap- easy to access and cultivate. ping mechanism known, the suction trap, which is far from being completely understood. We believe that it also holds ready ‘scientific surprises’ and hope to inspire Distribution and Life-forms of Utricularia future research on these still enigmatic and mechanically Utricularia can be found almost worldwide, with hotspots highly complex devices. of diversity in South America and Australia (Taylor 1989). Bladderworts occur rarely in arid regions as they need at least seasonal humidity to thrive. The widest distribution Carnivory in the Lentibulariaceae is shown by some aquatic or semi-aquatic species that Within the flowering plant family Lentibulariaceae (order can be found in the entire circumboreal region (Lloyd Lamiales), three carnivorous genera with different prey 1942; Taylor 1989; Barthlott et al. 2007). capture mechanisms exist. Genlisea (corkscrew plants) Bladderworts grow in diverse habitats, all being charac- feature sub-terrestrial eel-traps (Darwin 1875; Lloyd terized by soils or water poor in nutrients and sparse com- 1942; Fleischmann 2012a), Pinguicula (butterworts) petition. According to their habitat, species can be divided develop active sticky leaves (Darwin 1875; Lloyd 1942; into several life-forms, whereas the boundaries between Heslop-Harrison 1970)andUtricularia (bladderworts) these life-forms are often vague and intermediate forms 2 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 Poppinga et al. — Functional morphology and biomechanics of Utricularia suction traps exist (Brewer-Carias 1973; Van Steenis 1981; Taylor 1989; them as semi-aquatic or semi-terrestrial.
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